Camelus dromedarius) during prenatal life: A light and ...In this stage, the tongue was well...
Transcript of Camelus dromedarius) during prenatal life: A light and ...In this stage, the tongue was well...
Anat Histol Embryol. 2017;1–8. wileyonlinelibrary.com/journal/ahe | 1© 2017 Blackwell Verlag GmbH
Received:18November2016 | Accepted:10October2017DOI:10.1111/ahe.12321
O R I G I N A L A R T I C L E
Morphogenesis of lingual papillae of one- humped camel (Camelus dromedarius) during prenatal life: A light and scanning electron microscopic study
A. S. Abou-Elhamd1,2 | M. Abd-Elkareem1 | A. El-Zuhry Zayed1,2
1DepartmentofAnatomy,HistologyandEmbryology,FacultyofVeterinaryMedicine,UniversityofAssiut,Assiut,Egypt2DepartmentofMedicalBiology,JazanUniversity,Jazan,SaudiArabia
CorrespondenceAlaaSayedAbou-Elhamd,DepartmentofAnatomyandHistology,FacultyofVeterinaryMedicine,AssiutUniversity,Assiut,Egypt.Email: [email protected]
SummaryThis studywasmade on 24 camel fetuses of crown-rump vertebral length (CVRL)rangingfrom10.5cmto105cmCVRL(94–352daysold).Thesecamelfetuseswereclassifiedintothreegroupsrepresentingthethreetrimestersofprenatallife.Duringthefirsttrimester(94–142days),lingualpapillae(circumvallateandlentiformpapillae)weredemonstratedonthelingualroot,butlingualbodyandtheapexwerealmostfreeofpapillaeexceptforsomescatteredepithelialprojectionsespeciallynearthelateralbordersofthebody. Inthesecondtrimester (152–229days), the lentiformpapillaecoveredtheentirerootofthetongueexceptforareasoccupiedbythecircumvallatepapillae.Tastebudswithclearporeswereobservedforthefirsttimeinareasbetweenthecircumvallategustatoryfurrowandsurfaceepitheliumofthetongue.Inaddition,shortnumerousfiliformpapillaewereobservedontherostralpartofthelingualbodyand the lateralpartsof theapex.Fungiformpapillae,however,weredemonstratedamidstthefiliformpapillae.Inthistrimester,tastebudswerealsoseenonthetopofthefungiformpapillae.Inthethirdtrimester(256–352days),alllingualpapillaewereclearlydemonstratedonthedorsumoftheroot,bodyandapexofthetongue.Bothtypes of gustatory papillae (circumvallate and fungiform) hadwell-developed tastebuds.Mechanicalpapillae(filiformandlentiform)werewelldeveloped.Lentiformpa-pillaeoccupiedmostofthedorsalaspectoftheTorus linguae;theywerelargerinsizewithsemicircularapices.Filiformpapillae,however,werenumerousanddemonstratedheavilyonthelateralandrostralpartsofthebodyaswellasontheapexofthetongue.
1 | INTRODUCTION
Camelus dromedarius(one-humpedcamel)isamongthelargestmam-malianspecies,livesinregionswithhightemperatureanddryclimateand fed on thorny plants with rough and hard stems (Bello etal.,2012,2015).Thecamel’smouth isverysturdyandhasdevelopedaspecialfeaturetomaintainefficientfeedingontheseplants(Sui,Su,&Chen,1983).The tongue isamuscularorgancoveredbymucousmembranewithanumberofsalivaryglandsandnervesembeddedinbetweenthemuscletissues.Onthedorsalsurfaceofthetongue,thelingualmucosawas thrown intoprojections called the lingualpapil-lae (Dyce, Sack, &Wensing, 1996; Sisson &Grossman, 1975). Thelingual papillae fulfil diverse functions during food intake, transport
andswallowing(Abbateetal.,2008;Skieresz-Szewczyk&Jackowiak,2017).The lingualpapillae in camels, likeothermammalian species,were classified into mechanical and gustatory papillae. Mechanicalpapillae, as previously described, include filiform, lentiform, conicalandwart-likepapillae (Qayyum,Fatani,&Mohajir, 1988).Gustatorypapillaewithtastebudsarefungiformandcircumvallate(Erdunchaoluetal., 2001;Qayyumetal., 1988;Salehietal., 2010).Foliategusta-torypapillaedemonstratedinothervertebrates(Abbateetal.,2009,2010;Abd-Elnaeim,Zayed,&Leiser,2002)havenotbeendescribedin theone-humped camel (Dyceetal., 1996).Themorphogenesisofthetongueanditspapillaewasinvestigatedinvariousmammalssuchasmouse(Iwasaki,Okumura,&Kumakura,1999;Iwasaki,Yoshizawa,&Kawahara,1996),goats (Shawulu,Kwari,&Abgyal,2012),human
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(Bradley&Stern,1967),rabbit (Elnasharty,Sharaby,&El-Din,2013)and sheep (Hejazi&Baroughi,2013).Mostprevious studieson theprenatal development of the camel’s lingual papillae (Abd-Elnaeim,Kelany,Dorreia,&Abdel-Moneim,2008;Bello,Alimi,Umaru,&Onu,2015;Belloetal.,2014;Bello,Alimi,Sonfada,etal.,2015;Dougbag,1987a,b;Salehietal.,2010)describedindividual lingualpapillaeandhavenotgivenageneraloutlineoftheirmorphogenesisandtimingoftheirdifferentiation.Inourpreviousreport(Gad-Allah,Abou-Elhamd,Abdelmonem,&Zayed,2015),wediscussedtheveryearlystagesofdevelopment of the tongue of one-humped camel. The aim of thisstudywastocompleteourinvestigationaboutthemorphogenesisofthecamel’stongueanditspapillaeduringprenatallifeusinglightandscanningelectronmicroscopethatmayhelpinbetterunderstandingthe relationships between the lingual morphology and the feedinghabitsinthisuniquespecies.
2 | MATERIAL AND METHODS
This study was made on 24 camel fetuses of CVRL ranging from10.5cmCVRLto105cmCVRL.Theageof the fetuseswascalcu-latedusing theequation:Age=(CVRL+23.99)/0.366according toElwishy,Hemeida,Omar,Mobarak,andElSayed (1981).Camel fe-tuseswere collected fromCairo Slaughter house; then, theywereclassifiedintothreegroupsrepresentingthethreetrimestersofpre-natal life; ten in the first, nine in the second and five in the thirdtrimester.Fetuses in the first trimester rangedfrom10.5 to28cmCVRL(94–142days),inthesecondtrimesterfrom32to60cmCVRL(152–229days)whileinthethirdtrimestertheyrangedfrom70to105cmCVRL(256–352days).Afterinvestigationofthegrossmor-phologyofthewholetongue,smallpiecesofthelingualmucosaandunderlying lingual tissue in the root, body and apexof the tongueweretakenandprocessedforlightandscanningelectronmicroscopy.Forlightmicroscopy,smalltissueblockswerefixedinneutralbufferformalin, washed under tap water, dehydrated in graded ethanol,clearedinmethylbenzoateandembeddedinparaffinwax.Three-to
five-micrometre-thickparaffinsectionsweremadeandstainedwithhaematoxylinandeosin,trichrome,PASandalcianbluestains,thenexaminedandphotographedmicroscopically.Forscanningelectronmicroscopy, small tissue blocks with the covering lingual mucosawerefixedinmixtureofparaformaldehydesolution(2.5%)andglu-taraldehydesolution (2.5%) inphosphatebuffer (pH7.3) for24hr.Sampleswerethenwashed in0.1Mphosphatebuffer,dehydratedin ascendinggradesof ethanol, critical point-dried in liquid carbondioxideandthencoatedwithgoldpalladiusinsputteringdevice.ThesampleswerethenexaminedandphotographedusingJSM-5400LVScanningelectronmicroscopeoperatedat20KVintheEMCenterofAssiutUniversity.
Thestudywasconductedinaccordancewiththeapprovalandguide-linessetoutbytheEthicsCommissionatAssiutUniversityinEgypt.
3 | RESULTS
Thedromedarylingualpapillaepresentspecificgrossanatomicaldur-ingprenataldevelopment.
3.1 | First trimester (94–142 days)
The tongue appeared elongatedwith a flat surface and almost uni-forminthicknessandwidththroughoutitslength(Figures1aand2b).Lingualpapillaeweredemonstratedon the lingual root (2b). Lingualbodyandtheapexwerealmostfreeofpapillaeexceptforsomescat-teredepithelialprojectionsespeciallyonthelateralpartsofthedorsumof thebody.Theearly formed lingualgrooveappearedon themid-sagittallineoftheDorsum linguae(Figure2a,b).Thesurfaceepitheliumisformedofstratifiedcuboidalepithelium(Figure3a).Theprimordiaof circumvallate and lentiform papillae were clearly demonstratedonthelingualroot(Figure3a).Thecircumvallatepapillaappearedassmallprominencessurroundedbycirculargroovesandanannularpad(Figure3b). The circular groove of circumvallate papillawas formedasaresultofsequesteringepithelialcells(3c).Someepithelialplaco-desappearedonthelingualbodyresultingfromdifferentialepithelialgrowthrepresentingtheprimordiaoffungiformpapillae(Figure3d–f).
3.2 | Second trimester (152–229 days)
The tongue attained a more elongated form with tapering end(Figure1b). The covering lingual epithelium displayed the featuresof keratinized stratified squamous epitheliumonbothpapillary andinterpapillarydorsal lingualsurface.Thecircumvallateand lentiformpapillaeweredemonstratedonlyontherootofthetongue.Thelenti-formpapillaeappearedcoveringalltherootofthetongueexcepttheareaoccupiedbythecircumvallatepapillae,andtheywerearrangedlaterallyintworows(4–5each)oneithersideofthelingualroot.Theyappearedassmallprominencesurroundedbycirculargroovesandan-nularpadsofthesurroundinglingualmucosa(Figure4a,c).Tasteporeswereobservedintheareabetweenthecircumvallategustatoryfur-rowandthesurroundingsurfaceepitheliumofthetongue(Figure4b).
F IGURE 1 AGrossphotographshowingfetalcameltonguesatdifferentstagesofdevelopment:(a)(firsttrimester),(b)(secondtrimester)and(c)(thirdtrimester).Abbreviations:A;apex,B;body,R;root.NotetheprominentTorus linguaeintherootregioninthethirdtrimester
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Inthisstage,shortnumerousfiliformpapillae,whichappearedasdome-like elevations,were observed laterally on the rostral part ofthebodyandtheapexandofthetongue.Manythread-likeepithelialprojectionswereseenamongthem(Figure4f,g).Thefungiformpapil-laeweredemonstratedamidstthefiliformpapillae.Inthisstage,tastebudswerefirstseenonthetopofthesepapillaewithwell-demarcatedtastepores(Figure4e,h).
3.3 | Third trimester (256–352 days)
Inthisstage,thetonguewaswelldevelopedandattainedtheformof adult tongue with prominent Torus linguae. All lingual papil-lae were clearly demonstrated on the dorsum of the root, bodyand apex of the tongue (Figure1c). The gustatory papillae (cir-cumvallate and fungiform) hadwell-developed taste buds,whichshowed basal, supporting and neuroepithelial cells. The tasteporesweredemonstratedon the freeand lateral surfacesof thepapillae (Figure5a,c,e). Axons of neuroepithelial cells were seenpenetrating thesubepithelial connective tissue (Figure5c). Inad-dition, Ebner’s glandswerewell developed and their ductswereseenpenetratingthegustatoryfurrow(DataS1).TheseglandswerenegativetoPASandalcianbluereactions(DataS2).Thefungiformpapillaewereroundedandeachonewassurroundedbyapromi-nentgroove;tasteporesweredemonstratedontheirfreesurfaces.Lentiform papillae were numerous and larger in size with semi-circularapices (Figure5g), and theycoveralmostallof theTorus linguae except areas occupied by circumvallate papillae. Filiformpapillae, however, were more numerous and larger in size; theyweredemonstratedheavilyonthe lateralandrostralpartsofthebodyaswellasontheapex(Figure5f).
4 | DISCUSSION
Thepresentstudywascarriedouton24camelfetuses(94–352days)toinvestigatethedevelopmentalchangesinthetongueanditspapil-laeduringthethreetrimestersoftheprenatallife.
In agreementwith Saidu etal. (2015) and Bello,Alimi, Sonfada,etal.(2015),thetongueappearedelongatedwithflatsurfaceandal-mostuniformthicknessandwidththroughoutitslengthinallstagesofdevelopment.
Thecamellingualepithelium,asdemonstratedinthecurrentstudy,experiencedthefirstappearanceofpapillaewhenthisepitheliumat-tainedastratifiedform.SimilarconclusionhasbeenreportedbyHejaziandBaroughi(2013),whomentionedthatthetimeofemergenceandgrowthof the lingualpapillaeaccompanytheformationofstratifiedsquamousepithelium. InastudyontheGeomyid&Heteromyidro-dents(Frederick,Stangl,&Russell,1994)statedthatmechanicalpapil-laeare the firstdifferentiated lingualpapillaeandgustatorypapillaewithtastebudcellsarethelasttoappearandtheyemergenearthedelivery.Thelaststatementdisagreeswithourcurrentfindingswherethetimingofemergenceof lingualpapillae isaregional issuewherebothmechanicalandgustatorypapillaeappearedfirstonthelingualrootwhilethoseonthebodyandapexappearedlateron.Moreover,the fungiformpapillae (gustatorypapillae)preceded theappearanceoffiliformpapillae(mechanicalpapillae)onthebodyandapexofthecameltonguefetuses.
In agreement with previous studies (Erdunchaolu etal., 2001;Qayyum,Fatani,Mehta,Shaad,&Mustafa,1991;Saiduetal.,2015;Salehietal.,2010),thelingualpapillaeinadultcamelsincludefiliform,lentiform as mechanical papillae and fungiform and circumvallateasgustatorypapillae.Qayyumetal. (1991)describeda special type(wart-like)papillaeincloserelationshipwithcircumvallatepapillae.Inaddition,Ramayyaetal.(Ramayya,Babu,Rao,Lakshmi,&Patki,2012)reportedconicalpapillaeontheperipheryofthedorsalsurfaceofthetongue especially on the Torus linguae. According to Qayyum etal.(1988),thewart-likepapillaeseenontherootofthetonguecanbeclassifiedintotwomajortypes:withpointedandbluntends,respec-tively.Itisclearthatthereisacontroversyinthetypesofmechanicalpapillaedemonstratedonthelingualrootofthecamel.Inouropinionandaccordingtothecurrentfindings,thecamelhasonlytwotypesofmechanicalpapillae:oneonthebodyandapex (filiform)andoneontheroot(lentiformtype)whichsometimeshasapointedendanddescribedaswart-likeorbluntendanddescribedasconicalpapillabysomeauthors.Itseemsthatthesearesubtypesoflentiformpapillaewhichmaydeveloppostnatallyastheyhavenotbeendemonstratedinthecurrentprenatalstudy.
Thepresentstudyshowedthatthecircumvallatepapillaeappearedearlyinthefirsttrimesterassmallprominencessurroundedbycirculargrooves.Theywerearrangedintworows(4–5ineachraw)oneithersideoftheTorus linguaeinbetweenthedevelopinglentiformpapillae.Thenumberofthiskindofgustatorypapillaediffersgreatlyamongspe-cies(Agungpriyonoetal.,1995;Ateş,Bozkurt,Kozlu,Alan,&DÜzler,2013; Chamorro, De Paz, Sandoval, & Fernandez, 1986; Chamorro,Fernandez, De Paz, Pelaez, &Anel, 1994; Erdunchaolu etal., 2001;
F IGURE 2 Lightmicrograph(a)andscanningelectronmicrograph(b)offetalcameltonguesinthefirsttrimestershowinglingualpapillae(arrows)onthelingualroot(R).Lingualbody(B)andapex(A)arealmostfreeofpapillaeexceptforsomescatteredepithelialprojectionsespeciallyonthelateralaspectsofthebody.Theearlyformedlingualgrooveappearsonthemid-sagittallinein(b)(asterisks).Noticetheintrinsiclingualmuscle(ILM)andextrinsiclingualmuscle(ELM)in(a).(a)Isstainedwithhaematoxylinandeosin
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Fredericketal.,1994).Itcanbepostulatedthatanimalswithoutfoliategustatorypapillaelikecamelhavenumerouscircumvallatepapillaeincomparisonwiththosewhichhavefoliatepapillaelikeequines.
In the second trimester, tastebudswere firstobservedopeninginthelateralwallofthecircumvallatepapillae.Bythethirdtrimester,tastebudswereseenopeningonbothdorsalandlateralsurfacesofthepapillae.Inthesamecontext,Erdunchaoluetal.(2001)andBello,Alimi,Sonfada,etal.(2015)foundtastebudsonthelateralpapillarysurfacewhile (Doughbag, 1988; Salehi etal., 2010) observed tastebudsonthedorsalsurfaceofthecircumvallatepapillaeofdevelopingcameltongue.Inadultcamel,ElSharapy(ElSharaby,2006;ElSharaby,Alsafy,El-Gendy,&Wakisaka,2012)mentionedthatthefreesurfaceof thecircumvallatepapillae is freeof tasteporeandmostof themwerelocatedalongthemedialwallepitheliumandoccasionallyinthelateralwall.Thelastresultsinadultcamelsmaybeduetoapostnatal
modulationofthepapillaryepitheliumasaresultofcellularinvolutionthatmayaccompanyincreasingdepthsofthepapillarycirculargroovesduringpostnataldevelopment.
PrematureEbner’sglandswereobservedinthethirdtrimesterinthedeeperpartsofthecircumvallatepapillaeandtheywereopeningintothegustatoryfurrow.TheyshowednegativereactivitytoPASandalcianbluereactionindicatingthattheirsecretionsaremainlyserousand free frommucus contents. Sbarbati,Crescimanno, andOsculati(1999)statedthattheseglandsaremainlyinvolvedinthewashingofthevallumaroundthecircumvallatepapillae.Thelastauthorsaddedthat both circumvallate papillae and Ebner’s glands form a singlefunctionalunitywhichseemstorepresentanimportantenzyme-andpheromone-producing system composed of a sensitive (taste buds)and an effectory (Ebner’s gland) branch linked by feedbackmecha-nismsofcontrol.Theyhypothesizedthatthetastebudslocatedinthe
F IGURE 3 Lightandscanningelectronmicrographsoffetalcameltonguesatthefirsttrimestershowingthedevelopingcircumvallate(a,b,c)andfungiformpapillae(e,d,f,longarrows).Thesurfaceepitheliumisformedofstratifiedcuboidalepithelium.Theprimordiumofcircumvallatepapilla(bluearrow)andlentiformpapillae(bluearrowhead)isclearlydemonstratedontheroot(a)whiletheprimordiaoffungiformpapillaeappearonthebody(d)intheformofepithelialplacodes(blackarrows).Noticethatthecircumvallatepapillaappearsassmallprominencesurroundedbycirculargroove(arrowheads)andanannularpad(asterisks).(c)Demonstratesahighermagnificationoftheformingcirculargrooveofcircumvallatepapillabysequesteringepithelialcells(redarrows).(f)Demonstratesahighermagnificationofthedevelopingfungiformpapillaintheformofepithelialplacodethatresultsfromdifferentialepithelialgrowth.(a,d)Arestainedwithhaematoxylinandeosin
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distalportionoftheEbner’sglandsductalsystemcanbeconsideredsimilartothechemoreceptorcellslocatedinotherportionsofthedi-gestiveapparatussuchaspancreaticandbileducts.
In agreementwith that reportedbyGad-Allah etal. (2015), at94days of pregnancy, the primordia of the fungi papillae firstlyappeared on the apex of the camel tongue and the circumvallateand lentiform papillae on the root, however, filiform papillae ap-pearedlater.Thepresentfindingsrevealedthatfungiformpapillaeappeared as epithelial placodes in the first trimester and became
differentiatedgraduallyinthesecondtothethirdtrimester.Similartothatobservedincattle(Chamorroetal.,1986),thebactriancamel(Erdunchaolu etal., 2001), Akkaraman sheep (Ünsal, Aktumsek,Celik,&Sur,2003)andreeves’muntjacdeer (Zheng&Kobayashi,2006), dromedary camel (Sharifabad and Salehi, 2014), the tastebudswith taste poreswere demonstrated on the free surface ofthefungiformpapillae.Unlikely,fungiformpapillaeofgoat(Kumar,Kumar,& Singh, 1998;Kurtula&Atalgınb, 2008;Qayyum&Beg,1975),Japaneseweasels(Furubayashi,Sato,&Ishibashi,1989)and
F IGURE 4 Lightandscanningelectronmicrographsoffetalcameltonguesatthesecondtrimestershowingthepapillaeontheroot(circumvallate;a,c,dandlentiformpapillae;b)andpapillaeonthebody(Fungiform;e,handfiliformpapillaef,g).(d)Demonstratesahighermagnificationoftheareabetweenthecircumvallategustatoryfurrowandsurfaceepitheliumofthetongue.Abbreviations:AP(Annularpad),F(filiformpapillae),arrowheads(tastepores),asterisks(gustatoryfurrow).Notethekeratinizedcoveringepitheliumofthelingualpapillae.(a,b,e,f)Arestainedwithhaematoxylinandeosin
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Egyptian camel (Korans&Bachir, 2004)werewithout taste buds.The last finding that fungiform papillae in Egyptian camel lacktaste budsmaybe attributed to amisleading findingdue to non-representingtissuematerials.
Thepresent study revealed that the lentiformpapillaewere thefirstmechanicalpapillaeseenonthe lingualsurfaceofcamel in thefirsttrimester.InaccordancewithErdunchaoluetal.(2001),onlysim-pletypeof lentiformpapillaewasobservedonthedorsalsurfaceofthetongueofcamel.However,simpleandcompoundtypeof thesepapillaewasreportedincaprine(Kumaretal.,1998).
In thepresent study, the filiformpapillaebecameclearlyvisiblein the second trimester of prenatal life then they became heavilydemonstratedonthelateralandrostralpartsofthebodyaswellasontheapex.InaccordancewithQayyumetal.(1988),therewerenosecondarypapillaryprojections in the filiformpapillaeof the cameltongue.
In agreementwithHejazi andBaroughi (2013), keratinizationofpapillaryepitheliumwasdemonstratedduringembryoniclifeandthatthereisnorelationshipbetweentheirkeratinizationandthedietoftheanimalafterthebirth.
F IGURE 5 Lightandscanningelectronmicrographsoffetalcameltonguesatthethirdtrimestershowingthegustatory(circumvallatepapillaea-dandfungiforme,f)andmechanicalpapillae(filiformpapillae;e,fandlentiform;g).(d)Demonstratestastepores(asterisks)inthegustatoryfurrow(blackarrows)ofthecircumvallatepapillae.Insetin(a)showsahighermagnificationofthemarkedareawiththetastebudsofthecircumvallatepapilla.Noticethetastebudswiththeaxonsofneuroepithelialcellspenetratinginthesubepithelialconnectivetissuein(c)(blackarrowheads).Abbreviationsandshapes:annularpad(AP),Ebner’sgland(Eg),fungiformpapilla(redarrow),filiformpapillae(F),lentiformpapillae(L),tastebuds(bluearrowheads).(a,e)Arestainedwithhaematoxylinandeosin,while(c)isstainedwithtrichromestain
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ACKNOWLEDGEMENTS
We are grateful to the technician staffs of the Department ofAnatomy,HistologyandEmbryology,FacultyofveterinaryMedicine,AssiutUniversity,fortheirhelpandvaluabletechnicalassistance.TheprojectisfundedbyAssiutUniversity,Egypt.
CONFLICT OF INTEREST
Theauthorsdeclarenoconflictofinterest.
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How to cite this article:Abou-ElhamdAS,Abd-ElkareemM,El-ZuhryZayedA.Morphogenesisoflingualpapillaeofone-humpedcamel(Camelus dromedarius)duringprenatallife:Alightandscanningelectronmicroscopicstudy.Anat Histol Embryol. 2017;00:1–8. https://doi.org/10.1111/ahe.12321